Skip to main content

Lipid Metabolism, Compartmentalization and Signalling in the Regulation of Pollen Tube Growth

  • Chapter
  • First Online:
The Pollen Tube

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 3))

Abstract

To understand the biological context of lipid metabolism and signalling in pollen, we have to consider male gametophytes as organisms optimised for their role in sexual reproduction, but also for survival in dry conditions. While our knowledge of molecular mechanisms governing pollen development and pollen tube growth is based on the studies of a few model species (mostly Arabidopsis, tobacco, petunia and lily), important aspects of pollen development may vary substantially among species. Moreover, current understanding of pollen lipid biochemistry is rather fragmentary, since biochemically tractable amounts of pollen material are difficult to obtain, and knowledge of sporophytic lipid metabolism and signalling cannot be simply transferred to the study of male gametophytes.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anthony RG, Henriques R, Helfer A, Meszaros T, Rios G, Testerink C, Munnik T, Deak M, Koncz C, Bogre L (2004) A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. EMBO J 23:572–581

    Article  CAS  PubMed  Google Scholar 

  2. Baker H, Baker I (1979) Starch in angiosperm pollen grains and its anthecological significance. New Zeal J Bot 17:535

    Google Scholar 

  3. Bloch D, Lavy M, Efrat Y, Efroni I, Bracha-Drori K, Abu-Abied M, Sadot E, Yalovsky S (2005) Ectopic expression of an activated RAC in Arabidopsis disrupts membrane cycling. Mol Biol Cell 16:1913–1927

    Article  CAS  PubMed  Google Scholar 

  4. Bohme K, Li Y, Charlot F, Grierson C, Marrocco K, Okada K, Laloue M, Nogue F (2004) The Arabidopsis COW1 gene encodes a phosphatidylinositol transfer protein essential for root hair tip growth. Plant J 40:686–698

    Article  CAS  PubMed  Google Scholar 

  5. Braun M, Baluska F, von WM, Menzel D (1999) Redistribution of actin, profilin and phosphatidylinositol-4, 5-bisphosphate in growing and maturing root hairs. Planta 209:435–443

    Article  CAS  PubMed  Google Scholar 

  6. Brink R (1924) The influence of electrolytes on pollen tube development. J Gen Physiol 6:677–682

    Article  CAS  PubMed  Google Scholar 

  7. Bucher M, Brander KA, Sbicego S, Mandel T, Kuhlemeier C (1995) Aerobic fermentation in tobacco pollen. Plant Mol Biol 28:739–750

    Article  CAS  PubMed  Google Scholar 

  8. Carlton J, Cullen P (2005) Coincidence detection in phosphoinositide signaling. Trends Cell Biol 15:540–547

    Article  CAS  PubMed  Google Scholar 

  9. Clarke SR, Staiger CJ, Gibbon BC, Franklin-Tong VE (1998) A potential signaling role for profilin in pollen of Papaver rhoeas. Plant Cell 10:967–979

    Article  CAS  PubMed  Google Scholar 

  10. Carol RJ, Takeda S, Linstead P, Durrant MC, Kakesova H, Derbyshire P, Drea S, Zarsky V, Dolan LA (2005) A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature 438:1013–1016

    Article  CAS  PubMed  Google Scholar 

  11. Cole R, Synek L, Zarsky V, Fowler J (2005) SEC8, a Subunit of the Putative Arabidopsis Exocyst Complex, Facilitates Pollen Germination and Competitive Pollen Tube Growth. Plant Physiol 138:2005–2018

    Article  CAS  PubMed  Google Scholar 

  12. Cvrčkova F (2000) Are plant formins integral membrane proteins? Genome Biol 1:RESEARCH001

    PubMed  Google Scholar 

  13. Cvrčkova F, Novotny M, Pickova D, Zarsky V (2004a) Formin homology 2 domains occur in multiple contexts in angiosperms. BMC Genomics 5:44

    Google Scholar 

  14. Cvrčkova F, Rivero F, Bavlnka B (2004b) Evolutionarily conserved modules in actin nucleation: lessons from Dictyostelium discoideum and plants. Review article. Protoplasma 224:15–31

    Google Scholar 

  15. Czech MP (2003) Dynamics of phosphoinositides in membrane retrieval and insertion. Annu Rev Physiol 65:791–815

    Article  CAS  PubMed  Google Scholar 

  16. de Graaf BHJ, Cheung AY, Andreyeva T, Levasseur K, Kieliszewski M, Wu H (2005) Rab11 GTPase-Regulated Membrane Trafficking Is Crucial for Tip-Focused Pollen Tube Growth in Tobacco. Plant Cell 17:2564–2579

    Article  PubMed  Google Scholar 

  17. Deeks MJ, Hussey PJ, Davies B (2002) Formins: intermediates in signal-transduction cascades that affect cytoskeletal reorganization. Trends Plant Sci 7:492–498

    Article  CAS  PubMed  Google Scholar 

  18. Dhonukshe P, Baluska F, Schlicht M, Hlavacka A, Samaj J, Friml J, Gadella TW Jr (2006) Endocytosis of Cell Surface Material Mediates Cell Plate Formation during Plant Cytokinesis. Dev Cell 10:137–150

    Article  CAS  PubMed  Google Scholar 

  19. Dorne A, Kappler R, Kristen U, Heinz E (1988) Lipid-metabolism during germination of tobacco pollen. Phytochemistry 27:2027–2031

    Article  CAS  Google Scholar 

  20. Downes CP, Gray A, Lucocq JM (2005) Probing phosphoinositide functions in signaling and membrane trafficking. Trends Cell Biol 15:259–268

    Article  CAS  PubMed  Google Scholar 

  21. Elias M, Drdova E, Ziak D, Bavlnka B, Hala M, Cvrčkova F, Soukupova H, Zarsky V (2003) The exocyst complex in plants. Cell Biol Int 27:199–201

    CAS  Google Scholar 

  22. Elias M, Potocky M, Cvrčkova F, Zarsky V (2002) Molecular diversity of phospholipase D in angiosperms. BMC Genomics 3:2

    Article  PubMed  Google Scholar 

  23. Fiebig A, Mayfield JA, Miley NL, Chau S, Fischer RL, Preuss D (2000) Alterations in CER6, a gene identical to CUT1, differentially affect long-chain lipid content on the surface of pollen and stems. Plant Cell 12:2001–2008

    Article  CAS  PubMed  Google Scholar 

  24. Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    Article  CAS  PubMed  Google Scholar 

  25. Franklin-Tong V, Drobak B, Allan A, Watkins P, Trewavas A (1996) Growth of Pollen Tubes of Papaver rhoeas Is Regulated by a Slow-Moving Calcium Wave Propagated by Inositol 1,4,5-Trisphosphate. Plant Cell 8:1305–1321

    Article  CAS  PubMed  Google Scholar 

  26. Freeling M, Bennett D (1985) Maize Adh1. Annu Rev Genet 19:297–323

    CAS  PubMed  Google Scholar 

  27. Fujii H, Ichimori K, Hoshiai K, Nakazawa H (1997) Nitric oxide inactivates NADPH oxidase in pig neutrophils by inhibiting its assembling process. J Biol Chem 272:32773–32778

    Article  CAS  PubMed  Google Scholar 

  28. Gardiner JC, Harper JD, Weerakoon ND, Collings DA, Ritchie S, Gilroy S, Cyr RJ, Marc J (2001) A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane. Plant Cell 13:2143–2158

    Article  CAS  PubMed  Google Scholar 

  29. Gass N, Glagotskaia T, Mellema S, Stuurman J, Barone M, Mandel T, Roessner-Tunali U, Kuhlemeier C (2005) Pyruvate decarboxylase provides growing pollen tubes with a competitive advantage in petunia. Plant Cell 17:2355–2368

    Article  CAS  PubMed  Google Scholar 

  30. Golub T, Caroni P (2005) PI(4,5)P2-dependent microdomain assemblies capture microtubules to promote and control leading edge motility. J Cell Biol 169:151–165

    Article  CAS  PubMed  Google Scholar 

  31. Gupta R, Ting JTL, Sokolov LN, Johnson SA, Luan S (2002) A tumor suppressor homolog, AtPTEN1, is essential for pollen development in Arabidopsis. Plant Cell 14:2495–2507

    Article  CAS  PubMed  Google Scholar 

  32. Helsper J, Degroot P, Linskens H, Jackson J (1986) Phosphatidylinositol phospholipase-C activity in pollen of lilium-longiflorum. Phytochemistry 25:2053–2055

    Article  Google Scholar 

  33. Helsper J, Degroot P, Linskens H, Jackson J (1986b) Phosphatidylinositol monophosphate in lilium pollen and turnover of phospholipid during pollen-tube extension. Phytochemistry 25:2193–2199

    Google Scholar 

  34. Helsper J, Heemskerk J, Veerkamp J (1987) Cytosolic and particulate phosphatidylinositol phospholipase-C activities in pollen tubes of lilium-longiflorum. Physiologia Plantarum 71:120–126

    Article  CAS  Google Scholar 

  35. Huang S, Blanchoin L, Kovar DR, Staiger CJ (2003) Arabidopsis capping protein (AtCP) is a heterodimer that regulates assembly at the barbed ends of actin filaments. J Biol Chem 278:44832–44842

    Article  CAS  PubMed  Google Scholar 

  36. Hunt L, Otterhag L, Lee J, Lasheen T, Hunt J, Seki M, Shinozaki K, Sornmarin M, Gilmour D, Pical C, Gray J (2004) Gene-specific expression and calcium activation of Arabidopsis thaliana phospholipase C isoforms. New Phytol 162:643–654

    Article  CAS  Google Scholar 

  37. Hwang JU, Gu Y, Lee YJ, Yang Z (2005) Oscillatory ROP GTPase Activation Leads the Oscillatory Polarized Growth of Pollen Tubes. Mol Biol Cell 10 1091/mbc.E05–05-0409

    Google Scholar 

  38. Jackson J, Linskens H (1982) Conifer pollen contains phytate and could be a major source of phytate phosphorus in forest soils. Aust Forest Res 12:11–18

    Google Scholar 

  39. Jog SP, Garchow BG, Mehta BD, Murthy PPN (2005) Alkaline phytase from lily pollen: Investigation of biochemical properties. Arch Biochem Biophys 440:132–140

    Article  CAS  Google Scholar 

  40. Kawasaki T, Henmi K, Ono E, Hatakeyama S, Iwano M, Satoh H, Shimamoto K (1999) The small GTP-binding protein rac is a regulator of cell death in plants. Proc Natl Acad Sci USA 96:10922–10926

    Article  CAS  PubMed  Google Scholar 

  41. Kim HU, Hsieh K, Ratnayake C, Huang AHC (2002) A novel group of oleosins is present inside the pollen of Arabidopsis. J Biol Chem 277:22677–22684

    Article  CAS  PubMed  Google Scholar 

  42. Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua NH (1999) Rac homologues and compartmentalized phosphatidylinositol 4, 5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol 145:317–330

    Article  CAS  PubMed  Google Scholar 

  43. Kusner DJ, Barton JA, Qin C, Wang X, Iyer SS (2003) Evolutionary conservation of physical and functional interactions between phospholipase D and actin. Arch Biochem Biophys 412:231–241

    Article  CAS  PubMed  Google Scholar 

  44. Kusner DJ, Barton JA, Wen K, Wang X, Rubenstein PA, Iyer SS (2002) Regulation of phospholipase D activity by actin. Actin exerts bidirectional modulation of Mammalian phospholipase D activity in a polymerization-dependent, isoform-specific manner. J Biol Chem 277:50683–50692

    Article  CAS  PubMed  Google Scholar 

  45. Lalanne E, Honys D, Johnson A, Borner GH, Lilley KS, Dupree P, Grossniklaus U, Twell D (2004) SETH1 and SETH2, two components of the glycosylphosphatidylinositol anchor biosynthetic pathway, are required for pollen germination and tube growth in Arabidopsis. Plant Cell 16:229–240

    Article  CAS  PubMed  Google Scholar 

  46. Lemmon MA (2003) Phosphoinositide recognition domains. Traffic 4:201–213

    Article  CAS  PubMed  Google Scholar 

  47. Li DM, Sun H (1997) TEP1, encoded by a candidate tumor suppressor locus, is a novel protein tyrosine phosphatase regulated by transforming growth factor beta. Cancer Res 57:2124–2129

    CAS  PubMed  Google Scholar 

  48. Li H, Lin Y, Heath RM, Zhu MX, Yang Z (1999) Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell 11:1731–1742

    Article  CAS  PubMed  Google Scholar 

  49. Malhó R (1998) Role of 1,4,5-inositol triphosphate-induced Ca2+ release in pollen tube orientation. Sex Plant Reprod 11:231–235

    Article  Google Scholar 

  50. Mayfield JA, Fiebig A, Johnstone SE, Preuss D (2001) Gene families from the Arabidopsis thaliana pollen coat proteome. Science 292:2482–2485

    Article  CAS  PubMed  Google Scholar 

  51. Mellema S, Eichenberger W, Rawyler A, Suter M, Tadege M, Kuhlemeier C (2002) The ethanolic fermentation pathway supports respiration and lipid biosynthesis in tobacco pollen. Plant J 30:329–336

    Article  CAS  PubMed  Google Scholar 

  52. Moeder W, Yoshioka K, Klessig DF (2005) Involvement of the small GTPase Rac in the defense responses of tobacco to pathogens. Mol Plant Microbe In 18:116–124

    Article  CAS  Google Scholar 

  53. Monteiro D, Liu Q, Lisboa S, Scherer GEF, Quader H, Malhó R (2005) Phosphoinositides and phosphatidic acid regulate pollen tube growth and reorientation through modulation of [Ca2+]c and membrane secretion. J Exp Bot 56:1665–1674

    Article  CAS  PubMed  Google Scholar 

  54. Mueller-Roeber B, Pical C (2002) Inositol phospholipid metabolism in Arabidopsis. Characterized and putative isoforms of inositol phospholipid kinase and phosphoinositide-specific phospholipase C. Plant Physiol 130:22–46

    Article  CAS  PubMed  Google Scholar 

  55. Ohashi Y, Oka A, Rodrigues-Pousada R, Possenti M, Ruberti I, Morelli G, Aoyama T (2003) Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation. Science 300:1427–1430

    Article  CAS  PubMed  Google Scholar 

  56. Otterhag L, Sommarin M, Pical C (2001) N-terminal EF-hand-like domain is required for phosphoinositide-specific phospholipase C activity in Arabidopsis thaliana. FEBS Lett 497:165–170

    Article  CAS  PubMed  Google Scholar 

  57. Ovecka M, Lang I, Baluska F, Ismail A, Illes P, Lichtscheidl I (2005) Endocytosis and vesicle trafficking during tip growth of root hairs. Protoplasma 226:39–54

    Article  CAS  PubMed  Google Scholar 

  58. Pan Y, Wang X, Ma L, Sun D (2005) Characterization of phosphatidylinositol-Specific phospholipase C (PI-PLC) from Lilium daviddi pollen. Plant Cell Physiol doi:10.1093/pcp/pci181

    Google Scholar 

  59. Park J, Gu Y, Lee Y, Yang ZB, Lee Y (2004) Phosphatidic acid induces leaf cell death in Arabidopsis by activating the Rho-related small G protein GTPase-mediated pathway of reactive oxygen species generation. Plant Physiol 134:129–136

    Article  CAS  PubMed  Google Scholar 

  60. Pina C, Pinto F, Feijo JA, Becker JD (2005) Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol 138:744–756

    Article  CAS  PubMed  Google Scholar 

  61. Potocky M, Elias M, Profotova B, Novotna Z, Valentova O, Zarsky V (2003) Phosphatidic acid produced by phospholipase D is required for tobacco pollen tube growth. Planta 217:122–130

    CAS  PubMed  Google Scholar 

  62. Potocky M, Bezvoda R, Valentova O, Zarsky V (2004) Multiple phospholipase D isoforms are involved in regulation of polar growth in tobacco pollen tubes. Acta Physiol Plant 26S:156

    Google Scholar 

  63. Prado AM, Porterfield DM, Feijó JA (2004) Nitric oxide is involved in growth regulation and re-orientation of pollen tubes. Development 131:2707–2714

    Article  CAS  PubMed  Google Scholar 

  64. Preuss D, Lemieux B, Yen G, Davis RW (1993) A conditional sterile mutation eliminates surface components from Arabidopsis pollen and disrupts cell signaling during fertilization. Genes Dev 7:974–985

    Article  CAS  PubMed  Google Scholar 

  65. Rose P, Cutler A, Loewen M, Hogge L, Abrams S (1996) Metabolism and biological activity of (+)- and (−)-C-1′-O-methyl ABA in maize suspension-cell cultures. Phytochemistry 42:575–579

    Article  CAS  Google Scholar 

  66. Roth MG (2004) Phosphoinositides in constitutive membrane traffic. Physiol Rev 84:699–730

    Article  CAS  PubMed  Google Scholar 

  67. Routt SM, Bankaitis VA (2004) Biological functions of phosphatidylinositol transfer proteins. Biochem Cell Biol 82:254–262

    CAS  Google Scholar 

  68. Samaj J, Baluska F, Voigt B, Schlicht M, Volkmann D, Menzel D (2004) Endocytosis, actin cytoskeleton, and signaling. Plant Physiol 135:1150–1161

    Article  CAS  PubMed  Google Scholar 

  69. Samaj J, Read ND, Volkmann D, Menzel D, Baluska F (2005) The endocytic network in plants. Trends Cell Biol 15:425–433

    Article  CAS  PubMed  Google Scholar 

  70. Saunders CM, Larman MG, Parrington J, Cox LJ, Royse J, Blayney LM, Swann K, Lai FA (2002) PLC zeta: a sperm-specific trigger of Ca(2+) oscillations in eggs and embryo development. Development 129:3533–3544

    CAS  PubMed  Google Scholar 

  71. Schein M, Yang Z, Mitchell-Olds T, Schmid KJ (2004) Rapid evolution of a pollen-specific oleosin-like gene family from Arabidopsis thaliana and closely related species. Mol Biol Evol 21:659–669

    Article  CAS  Google Scholar 

  72. Suchy SF, Nussbaum RL (2002) The deficiency of PIP2 5-phosphatase in Lowe syndrome affects actin polymerization. Am J Hum Genet 71:1420–1427

    Article  CAS  PubMed  Google Scholar 

  73. Tadege M, Dupuis II, Kuhlemeier C (1999) Ethanolic fermentation: new functions for an old pathway. Trends Plant Sci 4:320–325

    Article  PubMed  Google Scholar 

  74. Testerink C, Munnik T (2005) Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci 10:368–375

    Article  CAS  PubMed  Google Scholar 

  75. van Leeuwen W, Okresz L, Bogre L, Munnik T (2004) Learning the lipid language of plant signalling. Trends Plant Sci 9:378–384

    Article  PubMed  Google Scholar 

  76. Vincent P, Chua M, Nogue F, Fairbrother A, Mekeel H, Xu Y, Allen N, Bibikova TN, Gilroy S, Bankaitis VA (2005) A Sec14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs. J Cell Biol 168:801–812

    Article  CAS  PubMed  Google Scholar 

  77. von Witsch M, Baluska F, Staiger CJ, Volkmann D (1998) Profilin is associated with the plasma membrane in microspores and pollen. Eur J Cell Biol 77:303–312

    Google Scholar 

  78. Wolters-Arts M, Lush WM, Mariani C (1998) Lipids are required for directional pollen-tube growth. Nature 392:818–821

    CAS  Google Scholar 

  79. Xu J, Brearley CA, Lin W, Wang Y, Ye R, Mueller-Roeber B, Xu Z, Xue H (2005) A role of Arabidopsis inositol polyphosphate kinase, AtIPK2alpha, in pollen germination and root growth. Plant Physiol 137:94–103

    Article  CAS  PubMed  Google Scholar 

  80. Yin HL, Janmey PA (2003) Phosphoinositide regulation of the actin cytoskeleton. Annu Rev Physiol 65:761–789

    Article  CAS  PubMed  Google Scholar 

  81. Yu JW, Mendrola JM, Audhya A, Singh S, Keleti D, DeWald DB, Murray D, Emr SD, Lemmon MA (2004) Genome-wide analysis of membrane targeting by S. cerevisiae pleckstrin homology domains. Mol Cell 13:677–688

    Article  CAS  PubMed  Google Scholar 

  82. Zarsky V, Elias M, Drdova E, Synek L, Quentin M, Kakesova H, Ziak D, Hala M, Soukupova H (2004) Do exocyst subunits in plants form a complex? Acta Physiol Plan 26S:146

    Google Scholar 

  83. Zhang W, Wang C, Qin C, Wood T, Olafsdottir G, Welti R, Wang X (2003) The oleate-stimulated phospholipase D, PLDdelta, and phosphatidic acid decrease H2O2-induced cell death in Arabidopsis. Plant Cell 15:2285–2295

    Article  CAS  PubMed  Google Scholar 

  84. Zhang W, Yu L, Zhang Y, Wang X (2005) Phospholipase D in the signaling networks of plant response to abscisic acid and reactive oxygen species. Biochim Biophys Acta 1736:1–9

    CAS  PubMed  Google Scholar 

  85. Zheng H, Rowland O, Kunst L (2005) Disruptions of the Arabidopsis Enoyl-CoA reductase gene reveal an essential role for very-long-chain fatty acid synthesis in cell expansion during plant morphogenesis. Plant Cell 17:1467–1481

    Article  CAS  PubMed  Google Scholar 

  86. Zhong R, Burk DH, Morrison WH3, Ye Z (2004) FRAGILE FIBER3, an Arabidopsis gene encoding a type II inositol polyphosphate 5-phosphatase, is required for secondary wall synthesis and actin organization in fiber cells. Plant Cell 16:3242–3259

    Article  CAS  PubMed  Google Scholar 

  87. Zhong R, Burk DH, Nairn CJ, Wood-Jones A, Morrison WH3, Ye Z (2005) Mutation of SAC1, an Arabidopsis SAC domain phosphoinositide phosphatase, causes alterations in cell morphogenesis, cell wall synthesis, and actin organization. Plant Cell 17:1449–1466

    Article  CAS  PubMed  Google Scholar 

  88. Zhong R, Ye Z (2004) Molecular and biochemical characterization of three WD-repeat-domain-containing inositol polyphosphate 5-phosphatases in Arabidopsis thaliana. Plant Cell Physiol 45:1720–1728

    Article  CAS  Google Scholar 

  89. Zonia L, Munnik T (2004) Osmotically induced cell swelling versus cell shrinking elicits specific changes in phospholipid signals in tobacco pollen tubes. Plant Physiol 134:813–823

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The related work in the author's laboratories was supported by EU-HPRN-CT-2002-00265, GAAV IAA6038410 and GACR 204/05/0268 grants.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. Žársky .

Editor information

Rui Malhó

Rights and permissions

Reprints and permissions

About this chapter

Cite this chapter

Žársky, V., Potocky, M., Baluška, F., Cvrčková, F. Lipid Metabolism, Compartmentalization and Signalling in the Regulation of Pollen Tube Growth. In: Malhó, R. (eds) The Pollen Tube. Plant Cell Monographs, vol 3. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_046

Download citation

Publish with us

Policies and ethics